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Functional Brain Circuitry Related to Arousal and Learning in Rats

  • Francisco Gonzalez-Lima

Abstract

The findings reviewed provide the first demonstration of how arousing and learning experiences modify the metabolic activity of the rat brain, and point to discrete functional pathways that seem to play key roles in the brain circuitry related to arousal and learning in mammals Autoradiographic 2-deoxyglucose (2DG) techniques were used to map the functional brain circuitry influenced by arousing electrical stimulation of the midbrain reticular formation (RET) in behaving rats. RET stimulation produced selective patterns of metabolic activation and suppression in discrete regions. The findings point to an integrative role of ascending and descending RET pathways in alerting and defensive reactions. During classical conditioning,involving an auditory stimulus and RET activation, metabolic changes were clearly different from those seen after RET stimulation alone. For example, opposite effects of learning and arousing conditions on the hippocampus were clearly discriminated. It is suggested that the structures affected by RET form part of the ascending reticular activating system and that some of these structures are also engaged in classical conditioning. Besides subserving arousal, the structures metabolically activated during conditioning may play different roles in signal learning, such as: Selective perception (auditory system), directed attention (prefrontal and posterior parietal cortex), motivation (thalamic and limbic structures), and temporal association of the conditioned and unconditioned CS-US stimulus pair (auditory nuclei, hippocampal formation). Finally, there are descending systems mediating the conditioned response made of mixed sensorimotor (flocculus, vestibular nuclei, central grey, spinal cord) and autonomic (medullary nuclei) components involved in the defensive “freezing” reaction to RET stimuli.

Keywords

Auditory Cortex Classical Conditioning Inferior Colliculus Vestibular Nucleus Hippocampal Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Basbaum AL, Fields HL (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Ann Rev Neurosci 7: 309–338PubMedCrossRefGoogle Scholar
  2. Birt D, Nienhuis R, Old J (1978) Effects of bilateral auditory cortex ablation on behavior and unit activity in rat inferior colliculus during differential conditioning. J Neurophysiol 41: 705–715PubMedGoogle Scholar
  3. Birt D, Olds ME (1982) Auditory response enhancement during differential conditioning in behaving rats. In: Woody CD (ed) Conditioning: representation of involved neural functions. Plenum Press, New York, pp 483–502Google Scholar
  4. Brodai A (1969) Neurological anatomy: in relation to clinical medicine. Oxford University Press, London Brudzynski SM, Mogenson GJ (1986) Decrease of locomotor activity by injections of carbachol into the anterior hypothalamic/preoptic area of the rat. Brain Res 376: 38–46Google Scholar
  5. Buchwald JS, Halas ES, Schramm S (1966) Changes in cortical and subcortical unit activity during behavioral conditioning. Physiol Behavl: 11–12Google Scholar
  6. Cajal S R y (1909) Histologie du Systeme nerveux de l’homme et des vertebras Consejo superior de investigaciones cientificas. Instituto Ramon y Cajal, MadridGoogle Scholar
  7. Caldecott-Hazard S, Mazziota J, Phelps M (1988) Cerebral correlates of depressed behavior in rats, visualized using 14C-2-deoxyglucose autoradiography. JNeurosci 8: 1951–1961Google Scholar
  8. Carstens E, Fraunhoffer M, Zimmermann M (1981) Serotonergic mediation of descending inhibition from midbrain periaqueductal gray, but not reticular formation, of spinal nociceptive transmission in the cat. Pain 10: 149–167CrossRefGoogle Scholar
  9. Chin JH, Killam EK, Killam KF (1965) Factors affecting sensory input in the cat: modification of evoked auditory potentials by reticular formation. Electroenceph Clin Neurophysiol 18: 567–574PubMedCrossRefGoogle Scholar
  10. Clemente CD (1968) Forebrain mechanisms related to internal inhibition and sleep. Cond Reflex 3: 145–174PubMedGoogle Scholar
  11. Coopersmith R, Lee S, Leon M (1986) Olfactory bulb responses after odor aversion learning by young rats. Develop Brain Res 24: 271–277CrossRefGoogle Scholar
  12. Delacour J (1984) Two neuronal systems are involved in a classical conditioning in the rat. Neurosci 13: 705–715CrossRefGoogle Scholar
  13. De Olmos J, Alheid GF, Beltramino CA (1985) Amygdala. In: Paxinos G (ed) The rat nervous system. Academic Press, Sydney, pp 223–334Google Scholar
  14. Eberhart JA, Morrell JI, Krieger MS, Pfaff DW (1985) An autoradiographic study of projections ascending from the midbrain central gray, and from the region lateral to it, in the rat. J Comp Neurol 241: 285310Google Scholar
  15. Edwards SB, De Olmos JS (1976) Autoradiographic studies of the projections of the midbrain reticular formation: ascending projections of nucleus cuneiformis. J Comp Neural 165: 417–432CrossRefGoogle Scholar
  16. Evans, EF, Nelson PG (1973) The responses of single neurones in the cochlear nucleus of the cat as a function of their location and the anaesthetic state. Exp Brain Res 17: 402–427PubMedGoogle Scholar
  17. Finkenstädt T, Ewert J-P (1985) Glucose utilization in the toad’s brain during anesthesia and stimulation of the ascending reticular arousal system. Naturwissenschaften 72: 161–162CrossRefGoogle Scholar
  18. Friedman HR, Janas J, Goldman-Rakic PS (1987) Metabolic activity in the thalamus and mammillary bodies of the monkey during spatial memory performance. Soc Neurosci Abstrl3: 207Google Scholar
  19. Fukushima K, Ohno M, Takahashi K, Kato M (1982) Location and vestibular responses of interstitial and midbrain reticular neurons that project to the vestibular nuclei in the cat. ErpBrain Res 45: 303–12Google Scholar
  20. Fuster JM (1982) Cortical neuron activity in the temporal organization of behavior. In: Woody CD (ed) Conditioning. representation of involved neural functions. Plenum Press, New York, pp 293–306Google Scholar
  21. Gallistel CR, Gomita Y, Yadin E, Campbell KA (1985) Forebrain origins and terminations of the medial forebrain bundle metabolically activated by rewarding stimulation or by reward-blocking doses of pimozide. JNeurosci 5: 1246–1261Google Scholar
  22. Glenn JF, Oatman LC (1980) Stimulation studies in the descending auditory pathway. Brain Res 196: 258–261PubMedCrossRefGoogle Scholar
  23. Glenn LL, Steriade M (1982) Discharge rate and excitability of cortically projecting intralaminar thalamic neurons during waking and sleep states. JNeurosci 2: 1387–1404Google Scholar
  24. Gomita Y, Gallistel CR (1982) Effects of reinforcement-blocking doses of pimozide on neural systems driven by rewarding stimulation of the MFB: A 14C-2-deoxyglucose analysis. Pharmacol Biochem Behav 17: 841–845PubMedCrossRefGoogle Scholar
  25. Gonzalez-Lima F (1986) Activation of substantia gelatinosa by midbrain reticular stimulation demonstrated with 2-deoxyglucose in the rat spinal cord. Neurosci Lett 65: 326–330PubMedCrossRefGoogle Scholar
  26. Gonzalez-Lima F (1987) Midbrain reticular stimulation produces patterns of metabolic activation and suppression in the cerebellum and vestibular nuclei: a 2-deoxyglucose study. Brain Res412: 275–284Google Scholar
  27. Gonzalez-Lima F (1988) Functional mapping of the brainstem during centrally evoked bradycardia: a 2deoxyglucose study. Behav Brain Res 28: 325–336PubMedCrossRefGoogle Scholar
  28. Gonzalez-Lima F, Scheich H (1984a) Functional activation in the auditory system of the rat produced by arousing reticular stimulation: a 2-deoxyglucose study. Brain Res 299: 201–214PubMedCrossRefGoogle Scholar
  29. Gonzalez-Lima F, Scheich H (1984b) Classical conditioning enhances auditory 2-deoxyglucose patterns in the inferior colliculus. Neurosci Lett 51: 79–85PubMedCrossRefGoogle Scholar
  30. Gonzalez-Lima F, Scheich H (1984c) Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. I: Activation of auditory nuclei. Behav Brain Res 14: 213–233PubMedCrossRefGoogle Scholar
  31. Gonzalez-Lima F, Scheich H (1985) Ascending reticular activating system in the rat: a 2-deoxyglucose study. Brain Res 344: 70–88PubMedCrossRefGoogle Scholar
  32. Gonzalez-Lima F, Scheich H (1986a) Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II: Auditory cortex plasticity. Behav Brain Res 20: 281–293PubMedCrossRefGoogle Scholar
  33. Gonzalez-Lima F, Scheich H (1986b) Classical conditioning of tone-signaled bradycardia modifies 2deoxyglucose uptake patterns in cortex, thalamus, habenula, caudate-putamen, and hippocampal formation. Brain Res 363: 239–356PubMedCrossRefGoogle Scholar
  34. Gonzalez-Lima F, Russell IS, Gonzalez-Lima EM (1986c) Representation of visual memory demonstrated with 2-deoxyglucose: lateralization of learning effects in split-chiasm rats. Neurosci Lett Supp 26: S620Google Scholar
  35. Gonzalez-Lima F, Russell IS, Gonzalez-Lima E (1987) Localization of neural substrates for visual memory demonstrated with 2-deoxyglucose. Neurosci Supp 22: S423Google Scholar
  36. Hart BL (1969) Experimental neuropsychology: a laboratory manual. Freeman, San Francisco Hebb DO (1949) The organization of behavior. a neuropsychological theory. Wiley, New York Hernandez-Peon R (1961) Reticular mechanisms of sensory control. In: Rosenblith WA (ed) Sensory communication. Wiley, New York, pp 497–520Google Scholar
  37. Hobson JA, Goldberg M, Vivaldi E, Riew D (1983) Enhancement of desynchronized sleep signs after pontine microinjection of the muscarinic agonist bethanechol. Brain Res 275: 127–136PubMedCrossRefGoogle Scholar
  38. Hyvärinen J, Poranen A, Jokinen Y (1980) Influence of attentive behavior on neuronal responses to vibration in primary somatosensory cortex of the monkey. JNeurophysiol43: 870–882 Ito M (1984) The cerebellum and neural control. Raven Press, New YorkGoogle Scholar
  39. Iwata J, LeDoux JE, Meeley MP, Arneric S, Reis DJ (1986) Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli. Brain Res 383: 195–214PubMedCrossRefGoogle Scholar
  40. John ER, Tang Y, Brill AB, Young R, Ono K (1986) Double-labeled metabolic maps of memory. Science 233: 1167–1175PubMedCrossRefGoogle Scholar
  41. Juliano SL, Whitsel BL (1987) A combined 2-deoxyglucose and neurophysiological study of primate somatosensory cortex. J Comp Neurol 263: 514–525PubMedCrossRefGoogle Scholar
  42. Kapp BS, Pascoe JP, Bixler MA (1984) The amygdala: a neuroanatomical systems approach to its contributions to aversive conditioning. In: Butters N, Squire LR (eds) The neuropsychology of memory. The Guilford Press, New YorkGoogle Scholar
  43. Kawasaki H, Watanabe S, Ueki S (1980) Potentiation of pressor and behavioral responses to brain stimulation following bilateral olfactory bulbectomy in freely moving rats. Brain Res Bull 5: 711–718PubMedCrossRefGoogle Scholar
  44. Keene JJ (1973) Reward-associated inhibition and pain-associated excitation lasting seconds in single intralaminar thalamic units. Brain Res 64: 211–224PubMedCrossRefGoogle Scholar
  45. Keene JJ (1975) Reward-associated excitation and pain-associated inhibition lasting seconds in rat medial pallidal units. Exp Neural 49: 97–114CrossRefGoogle Scholar
  46. Keene JJ (1978) Affect-related unit activity in forebrain. Fed Proc 37: 2246–2250PubMedGoogle Scholar
  47. Kelly JB (1974) Polysensory cortical lesions and auditory temporal pattern discrimination in the cat. Brain Res 80: 317–327PubMedCrossRefGoogle Scholar
  48. Kohnstamm O, Quensel F (1908) Centrum receptorium der Formatio reticularis and gekreutzt aufsteigenden Bahnen. Dtsch ZNeivenhk 36: 182–188Google Scholar
  49. König JFR, Klippel RA (1963) The rat brain:a stereotaxic atlas. Williams &Wilkins, BaltimoreGoogle Scholar
  50. Kryter KD (1979) Extraauditory effects of noise. In: Henderson D, Hamernik RP, Dosanjh DS, Mills JH (eds) Effects of noise on hearing. Raven Press, New York, pp 531–546Google Scholar
  51. Laroche S, Neuenschwander-El Massioui N, Edeline JM, Dutrieux G (1987) Hippocampal associative cellular responses: dissociation with behavioral responses revealed by a transfer-of-control technique. Behav Neural Bio1 47: 356–368CrossRefGoogle Scholar
  52. LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. JNeurosci 4: 683–698Google Scholar
  53. Levy WB, Steward 0 (1983) Temporal contiguity requirements for long-term associate potentiation/ depression in the hippocampus. Neurosci 8: 791–797Google Scholar
  54. Lorente de No R (1949) The structure of the cerebral cortex. In: Fulton JF (ed) Physiology of the nervous system. Oxford Univ Press, New York, pp 288–330Google Scholar
  55. Malmo RB, Mundt WL (1983) Cardiovascular and respiratory responses to electrical stimulation of the midbrain in the rat. Int J Psychophysiol 1: 75–81PubMedCrossRefGoogle Scholar
  56. Markowitsch HJ (1982) Thalamic mediodorsal nucleus and memory: a critical evaluation of studies in animals and man. Neurosci BiobehavRev6: 351–380Google Scholar
  57. Mesulam MM (1983) The functional anatomy and hemispheric specialization for directed attention. TINS 6: 384–387Google Scholar
  58. Miller JM, Pfingst BE, Ryan AF (1982) Behavioral modification of response characteristics of cells in the auditory system. In: Woody CD (ed) Conditioning. representation of involved neural functions Plenum Press, New York, pp 345–362Google Scholar
  59. Molnar M, Karmos G, Csepe V (1982) Intracortical auditory evoked potentials in the sleep-waking cycle of the cat. In: Sinz R, Rosenzweig MR (eds) Psychophysiology 1980. VEB Gustav Fischer-Verlag, Jena, and Elsevier, Amsterdam, pp 549–555Google Scholar
  60. Moruzzi G, Magoun HW (1949) Brain stem reticular formation and activation of the EEG. Electroenceph din Neurophysiol 1: 455–473Google Scholar
  61. Nauta WJH, Kuypers H (1958) Some ascending pathways in the brain stem reticular formation. In: Jasper HH, Protor L (eds) Reticular formation of the brain. Little-Brown, Boston, pp 3–30Google Scholar
  62. Nudo R, Masterton RB (1986) Stimulation-induced [14C]2-deoxyglucose labeling of synaptic activity in the central auditory system. J Comp Neural 245: 553–565CrossRefGoogle Scholar
  63. Olton DS, Meck WH, Church RM (1987) Separation of hippocampal and amygdaloid involvement in temporal memory dysfunctions. Brain Res 404: 180–188PubMedCrossRefGoogle Scholar
  64. Osen KK, Mugnaini E (1981) Neuronal circuits in the dorsal cochlear nucleus. In: Syka J, Aitkin L (eds) Neuronal mechanisms of hearing Plenum Press, New York, pp 119–125Google Scholar
  65. Pizzolato G, Soncrant TT, Holloway HW, Rapoport SI (1985) Reduced metabolic response of the aged rat brain to haloperidol. JNeurosci 11: 2831–2838Google Scholar
  66. Ramm P, Frost BJ (1983) Regional metabolic activity in the rat brain during sleep-wake activity. Sleep 6: 196–216PubMedGoogle Scholar
  67. Ramm P, Frost BJ (1986) Cerebral and local cerebral metabolism in the cat during slow wave and REM sleep. Brain Res 365: 112–124PubMedCrossRefGoogle Scholar
  68. Ropert N, Steriade M (1981) Input-output organization of the midbrain reticular core. J Neurophysiol 46: 17–31PubMedGoogle Scholar
  69. Rosenzweig MR, Bennett EL (1976) Neural mechanisms of learning and memory. MIT Press, CambridgeGoogle Scholar
  70. Russell IS (1980) Encephalization and neural mechanisms of learning. In: Jeeves M (ed) Psychology survey Na 3. Allen & Unwin, London, pp 92–114Google Scholar
  71. Ryan AF, Sharp FR (1982) Localization of (3H)2-deoxyglucose at the cellular level using freeze dried tissue and dry-looped emulsion. Brain Res 252: 177–180PubMedCrossRefGoogle Scholar
  72. Sasaki K, Shimono T, Oka H, Yamamoto T, Matsuda Y (1976) Effects of stimulation of the midbrain reticular formation upon thalamocortical neurones responsible for cortical recruiting responses.Brain Res 26: 261–273Google Scholar
  73. Scheibel, ME, Scheibel AB (1958) Structural substrates for integrative patterns in the brain stem reticular core. In: Jasper H, Proctor LD, Knighton RS, Noshay WS, Costello RT (eds) Reticular formation of the brain. Little Brown, Boston, pp 31–55Google Scholar
  74. Segundo JP, Arana R, French JD (1955) Behavioral arousal by stimulation of the brain in the monkey. J Neurosurg 12: 601–613PubMedCrossRefGoogle Scholar
  75. Sharp FR, Ryan AF (1984) Regional (14C)2-deoxyglucose uptake during forelimb movements evoked by rat motor cortex stimulation: pons, cerebellum, medulla, spinal cord, and muscle. J Comp Neural 224: 286–306CrossRefGoogle Scholar
  76. Sharp FR, Ryan AF, Goodwin P, Woolf NK (1981) Increasing intensities of wide band noise increase (14C)-2-deoxyglucose uptake in gerbil central auditory structures. Brain Res 230: 87–96PubMedCrossRefGoogle Scholar
  77. Shute CCD (1973) Cholinergic pathways in the brain. In: Laitinen LV, Livingston KE (eds) Surgical approaches in psychiatry. Univ Park Press, BaltimoreGoogle Scholar
  78. Sokoloff L (1984) Modeling metabolic processes in the brain in vivo. Ann Neural Suppl 15: Sl-S11Google Scholar
  79. Sokoloff L, Reivich M, Kennedy C, DesRosiers MH, Patlak CS, Pettigrew KD, Sakurada O, Shinohara M (1977) The (14C)deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28: 897–916PubMedCrossRefGoogle Scholar
  80. Steriade M (1980) State-dependent changes in the activity of rostral reticular and thalamocortical elements. In: Hobson JA, Scheibel AB (eds) The brainstem core: sensorimotor integration and behavioral state control. Neurosci Res Progr Bull 18. MIT Press, Cambridge, pp 83–91Google Scholar
  81. Steriade M, Ropert N, Kitsikis A, Oakson G (1980) Ascending activating neuronal networks in midbrain reticular core and related rostral systems. In: Hobson JA, Brazier MAB (eds) The reticular formation revisited. Raven Press, New York, pp 125–167Google Scholar
  82. Taniguchi I (1980) Changes in metabolic activity in the inferior colliculus following removal of auditory input. Biomed Rest 510–516Google Scholar
  83. Theurich M, Müller CM, Scheich H (1984) 2-deoxyglucose accumulation parallels extracellularly recorded spike activity in the avian auditory neostriatum. Brain Res 322: 157–161Google Scholar
  84. Thompson RF, Berger TW, Berry SD, Clark GA, Kettner RN, Lavond DG, Mauk MD, McCormick DA, Solomon PR, Weisz DJ (1982) Neuronal substrates of learning and memory: hippocampus and other structures. In: Woody CD (ed) Conditioning: representation of involved neural functions. Plenum Press, New York, pp 115–130Google Scholar
  85. Turner BH, Zimmer J (1984) The architecture and some of the interconnections of the rat’s amygdala and lateral periallocortex. J Comp Neural 227: 540–557CrossRefGoogle Scholar
  86. Versteeg CAM, Bohus B, De Jong W (1982) Attenuation by arginine and desglycinamide-lysinevasopressin of a centrally evoked pressor response. JAut New Syst 6: 253–262Google Scholar
  87. Voronin LL (1983) Long-term potentiation in the hippocampus. Neurosci 10: 1051–1069CrossRefGoogle Scholar
  88. Weinberger NM, Diamond DM (1987) Physiological plasticity in auditory cortex: rapid induction by learning. Prog in Neurobiol 29:1-SSGoogle Scholar
  89. Winsky L, Schindler CW, McMaster SE, Welsh JP, Harvey JA (1986) Enhanced uptake of 14C-2-deoxy-Dglucose (2DG) in the dorsal cochlear nucleus during Pavlovian conditioning. Soc Neurosci Abstr 12: 181Google Scholar
  90. Winson J, Abzug C (1978) Neuronal transmission through hippocampal pathways dependent on behavior. J Neurophysi of 41: 716–732Google Scholar
  91. Woolf NK, Sharp FR, Davidson TM, Ryan AF (1983) Cochlear and middle ear effects on metabolism in the central auditory pathway during silence: a 2-deoxyglucose study. Brain Res 274: 119–127PubMedCrossRefGoogle Scholar
  92. Young ED, Voigt HF (1981) The internal organization of the dorsal cochlear nucleus. In: Syka J, Aitkin L (eds) Neuronal mechanisms of hearing. Plenum Press, New York, pp 127–133Google Scholar

Copyright information

© Springer Science+Business Media New York 1989

Authors and Affiliations

  • Francisco Gonzalez-Lima
    • 1
  1. 1.Department of Anatomy, College of MedicineTexas A&M UniversityCollege StationUSA

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